Metabolic and molecular basis for the salt and alkali responses of Suaeda corniculata
Introduction
Saline-alkali soil is one of the major abiotic stresses limiting plant growth and crop productivity worldwide (Rana et al., 2008; Tavakkoli et al., 2011; Tuteja, 2007). Alkaline soil contains high levels of Na2CO3 and NaHCO3, which leads to a high pH (>9.0) (Zhang et al., 2016). In northeastern China, alkalinized grasslands have reached more than 70% coverage due to the presence of excessive alkaline salts (Zhang et al., 2013). Compared to neutral salt, alkali salt induces high pH and imposes more severe damage to plants (Yang et al., 2007). A high pH environment surrounding plant roots has a great impact on nutrient uptake, organic acid balance, ion homeostasis, and especially pH stability in cells (Guo et al., 2010; Wang et al., 2009). Thus, it is urgently important to determine how plants respond to and tolerate alkali stress, which would help plants adapt to stressful environments. To date, plant salt tolerance has been extensively studied, but alkali tolerance is not understood.
Alkali stress largely affects the cellular metabolism of plants primarily due to the high pH shock and excess accumulation of inorganic ions attenuating protein synthesis in plant tissue (Hu et al., 2019). Even in the halophyte Helianthus annuus, which has high resistance to saline conditions, the protein concentration was drastically decreased upon Na2CO3 treatment (Manivannan et al., 2008). Nevertheless, several studies demonstrated that plants could modulate their metabolic function to overcome such an unfriendly environment. It has been revealed that an enhanced energy supply and the activation of multiple antioxidants play important roles in the Puccinellia tenuiflora response to alkali stress (Yu et al., 2013). In Na2CO3-treated seedlings of H. tuberosus, proteins involved in glycolysis, the TCA cycle, the PSI system, ROS scavenging and signal transduction were induced by alkali stress (Zhang et al., 2016). In addition, metabolic analysis in Malus halliana showed that the abundances of sucrose, amino acids, alkaloids, flavonoids and carotenoids were significantly upregulated, which contributes to improving the saline-alkali resistance of M. halliana by maintaining a balanced redox state (Jia et al., 2020).
Suaeda species are annual euhalophytes with highly succulent leaves that are able to accommodate salt, and they are important halophyte resources naturally distributed in saline and alkaline soils throughout the world (Flowers and Colmer, 2008). Based on an analysis under neutral salt stress, more than twenty species of Suaeda have been reported for their ability to survive in extremely saline soil, achieving benefits derived from the specific physiological and molecular regulation of Suaeda plants (Diao et al., 2021; Hasanuzzaman et al., 2014; Liu et al., 2018; Yuan et al., 2018). Most studies focused on S. salsa, and several salt tolerance genes were characterized, including aquaporins (AQPs) (Qi et al., 2009), vacuolar Na+/H+ antiporters (Qiu et al., 2007), V-ATPase and V-PPase (Wang et al., 2001), indicating that Suaeda plants could modulate water potential and ion distribution by succulent leaf to compartment excess Na+. Osmotic adjustment also plays a critical role in Suaeda adapting to high salt conditions, the accumulation of proline and soluble sugars could effectively promote osmoregulation (Behr et al., 2017). In addition, the overall increase in antioxidant system activity, including the enzymes SOD, POD, CAT, and GPX, and metabolites such as glutathione, ascorbate, flavonoids and phenylpropanoids, facilitates tolerance to salinity in Suaeda (Wu et al., 2011). Moreover, the fluctuation of plant hormones in Suaeda under salt stress may be involved in the regulation of salt tolerance (Guo et al., 2019).
S. corniculata, a member of the Suaeda genus, shows a higher alkali tolerance than S. salsa and can survive in saline-sodic soil with pH values ranging from 10 to 15.5 (Liu et al., 2011). However, the underlying mechanisms of the S. corniculata response to alkali stress are not well understood. Plant roots act as the primary site for perceiving salt signals, and their physiological and metabolic activities largely reflect the regulatory information dictating how plants adapt to stressful environments. Here, we investigated the comprehensive response of S. corniculata roots to NaCl and NaHCO3 treatment via combined analysis of gene expression, metabolic pathways and protein profiles. The modulation of ROS scavenging, osmotic homeostasis, and reprogramming of multiple metabolic pathways jointly played important roles in the S. corniculata response to salt and alkali stress, which provides new insight into the fitness mechanism of S. corniculata under adverse conditions.
Section snippets
Plant material, growth condition, and stress treatment
Seeds of S. corniculata with same genetic background were collected from a saline-alkali soil area located in Zhaodong, Heilongjiang Province, Northeast China. Seedlings were sown in plastic pots filled with aseptic vermiculite and fertile black soil (2:1) in a greenhouse at 25/20 °C (day/night) with an 8 h light/16 h dark photoperiod, photosynthetically active radiation at 150 μmol m−2·s-1 and 50–70% relative humidity and were irrigated daily with half strength Hoagland’s solution (pH 6.21 ±
Effect of NaCl and NaHCO3 stress on root growth
We examined root growth and oxidative damage to evaluate the physiological impact induced by NaCl and NaHCO3 stress in S. corniculata. As the fresh biomass showed, the root growth was slightly affected by both the salt and alkali stress (Fig. 1), and even the dry weight displayed no significant difference between the treated plants and control, the fresh weight was obviously reduced after NaHCO3 stress for 3, 5, and 7 days (Fig. 1a, b), suggesting that the alkali treatment caused more severe
Alkali salt is more likely to cause severe stress than neutral salt
The activity of the root system under stress conditions is critical for plant survival and growth (Zhao et al., 2016). As a halophyte, S. corniculata has high tolerance to alkaline stress. S. corniculata plants grew well under 50 mM Na2CO3 (pH 11.0) and could tolerate up to 300 mM NaHCO3 (pH 11.0) for at least 18 days in our past experiments (Wei et al., 2012). Consistently, we found that the root fresh weight was slightly inhibited under 150 mM NaHCO3 for more than 3 days (Fig. 1a). The
Conclusion
In this study, we performed integrated physiology, proteomic and metabolomic analyses to examine the different molecular mechanisms in the S. corniculata roots response to salt and alkali stress. Our findings showed sophisticated and distinct metabolic and molecular regulation of salt and alkali responses in plants. In contrast to salt stress, many biology functional pathways have different respond under alkali stress, such as carbohydrate metabolism, fatty acid metabolism, antioxidant system,
Author contributions
Qiuying Pang designed the experiments and supervised the project. Wei Zang, Rongqing Miao, Yue Zhang, Yue Yuan performed the research and integrated the data. Wei Zang wrote the draft. Wei Zang, Rongqing Miao, Zhiqiang Zhou and Qiuying Pang finalized the data interpretation and the manuscript. All authors reviewed and approved the manuscript.
Declaration of Competing Interest
The authors declare no conflicts of interest.
Acknowledgement
This work was supported by the National Natural Science Foundation of China (No. 32070350 and No.31300305).
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These authors contributed equally to this work.